The rates of postmortem proteolysis of glutamate transporters differ dramatically between cells and between transporter subtypes

Journal of Histochemistry and Cytochemistry

Volumn 60, Issue 11, 2012, Pages 811-821

  Li, Yuchuan ^a,b   Zhou, Yun ^b   Danbolt, Niels Christian ^b  

^a ZHENGZHOU UNIVERSITY   (China)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

Glutamate transporter; Knockout mice; Postmortem proteolysis; Slc1a1; Slc1a2; Slc1a3

Indexed keywords

EPITOPE; EXCITATORY AMINO ACID TRANSPORTER 1; PROTEIN ANTIBODY; VESICULAR GLUTAMATE TRANSPORTER 1; EXCITATORY AMINO ACID TRANSPORTER 2; GLUTAMATE TRANSPORTER; SLC1A3 PROTEIN, MOUSE;

AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; BRAIN TISSUE; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; MOUSE; NONHUMAN; POSTMORTEM CHANGE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN TRANSPORT; TISSUE SECTION; ANIMAL; BRAIN; C57BL MOUSE; CADAVER; CYTOLOGY; IMMUNOHISTOCHEMISTRY; METABOLISM; PATHOLOGY; WESTERN BLOTTING;

MUS;

AMINO ACID TRANSPORT SYSTEM X-AG; ANIMALS; BLOTTING, WESTERN; BRAIN; EXCITATORY AMINO ACID TRANSPORTER 1; EXCITATORY AMINO ACID TRANSPORTER 2; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; POSTMORTEM CHANGES; PROTEOLYSIS;

EID: 84867417986     PISSN: 00221554     EISSN: None     Source Type: Journal    
DOI: 10.1369/0022155412458589     Document Type: Article

References (59)

1. Banner SJ, Fray AE, Ince PG, Steward M, Cookson MR, Shaw PJ. 2002. The expression of the glutamate re-uptake transporter excitatory amino acid transporter 1 (EAAT1) in the normal human CNS and in motor neurone disease: an immunohistochemical study. Neuroscience. 109:27-44.
2. Beart PM, O'Shea RD. 2007. Transporters for L-glutamate: an update on their molecular pharmacology and pathological involvement. Br J Pharmacol. 150:5-17.
3. Beckstrøm H, Julsrud L, Haugeto Ø, Dewar D, Graham DI, Lehre KP, Storm-Mathisen J, Danbolt NC. 1999. Interindividual differences in the levels of the glutamate transporters GLAST and GLT, but no clear correlation with Alzheimer's disease. J Neurosci Res. 55:218-229.
4. Bergles DE, Diamond JS, Jahr CE. 1999. Clearance of glutamate inside the synapse and beyond. Curr Opin Neurobiol. 9:293-298.
5. Bjørås M, Gjesdal O, Erickson JD, Torp R, Levy LM, Ottersen OP, Degree M, Storm-Mathisen J, Seeberg E, Danbolt NC. 1996. Cloning and expression of a neuronal rat brain glutamate transporter. Brain Res Mol Brain Res. 36:163-168.
6. Bjørnsen LP, Eid T, Holmseth S, Danbolt NC, Spencer DD, de Lanerolle NC. 2007. Changes in glial glutamate transporters in human epileptogenic hippocampus: inadequate explanation for high extracellular glutamate during seizures. Neurobiol Dis. 25:319-330.
7. Boston-Howes W, Gibb SL, Williams EO, Pasinelli P, Brown RH, Trotti D. 2006. Caspase-3 cleaves and inactivates the glutamate transporter EAAT2. J Biol Chem. 281:14076-14084.
8. Chen WZ, Mahadomrongkul V, Berger UV, Bassan M, Desilva T, Tanaka K, Irwin N, Aoki C, Rosenberg PA. 2004. The glutamate transporter GLT1a is expressed in excitatory axon terminals of mature hippocampal neurons. J Neurosci. 24:1136-1148.
9. Conti F, Weinberg RJ. 1999. Shaping excitation at glutamatergic synapses. Trends Neurosci. 22:451-458.
10. Danbolt NC. 2001. Glutamate uptake. Prog Neurobiol. 65:1-105.
11. Danbolt NC, Lehre KP, Dehnes Y, Chaudhry FA, Levy LM. 1998. Localization of transporters using transporter-specific antibodies. Methods Enzymol. 296:388-407.
12. Danbolt NC, Pines G, Kanner BI. 1990. Purification and reconstitution of the sodium-and potassium-coupled glutamate transport glycoprotein from rat brain. Biochemistry. 29:6734-6740.
13. Danbolt NC, Storm-Mathisen J, Kanner BI. 1992. An [Na++ K+] coupled L-glutamate transporter purified from rat brain is located in glial cell processes. Neuroscience. 51:295-310.
14. Dehnes Y, Chaudhry FA, Ullensvang K, Lehre KP, Storm-Mathisen J, Danbolt NC. 1998. The glutamate transporter EAAT4 in rat cerebellar Purkinje cells: a glutamate-gated chloride channel concentrated near the synapse in parts of the dendritic membrane facing astroglia. J Neurosci. 18:3606-3619.
15. Desilva T, Borenstein N, Volpe J, Kinney H, Rosenberg P. 2012. Expression of EAAT2 in neurons and protoplasmic astrocytes during human cortical development. J Comp Neurol. Epub Apr 23.
16. Figiel M, Allritz C, Lehmann C, Engele J. 2007. Gap junctional control of glial glutamate transporter expression. Mol Cell Neurosci. 35:130-137.
17. Fray AE, Ince PG, Banner SJ, Milton LD, Usher PA, Cookson MR, Shaw PJ. 1998. The expression of the glial glutamate transporter protein EAAT2 in motor neuron disease: an immunohistochemical study. Eur J Neurosci. 10:2481-2489.
18. Furness DN, Dehnes Y, Akhtar AQ, Rossi DJ, Hamann M, Grutle NJ, Gundersen V, Holmseth S, Lehre KP, Ullensvang K, et al. 2008. A quantitative assessment of glutamate uptake into hippocampal synaptic terminals and astrocytes: new insights into a neuronal role for excitatory amino acid transporter 2 (EAAT2). Neuroscience. 157:80-94.
19. Gegelashvili G, Danbolt NC, Dehnes Y, Balazs R, Cribbs DH, Cotman CW, Rodriguez-Kern A, Gegelashvili M. 2002. Caspasedependent regulation and receptor-like properties of glutamate transporters. Society for Neuroscience Abstracts. 28:441.16.
20. Gegelashvili M, Rodriguez-Kern A, Dehnes Y, Danbolt NC, Balazs R, Cribbs DH, Cotman CW, Gegelashvili G. 2002. Glutamate transporters: caspase-dependent regulation and receptor-like properties. Neuropharmacology. 43:287.
21. Haugeto Ø, Ullensvang K, Levy LM, Chaudhry FA, Honoré T, Nielsen M, Lehre KP, Danbolt NC. 1996. Brain glutamate transporter proteins form homomultimers. J Biol Chem. 271:27715-27722.
22. Holmseth S, Dehnes Y, Bjørnsen LP, Boulland JL, Furness DN, Bergles D, Danbolt NC. 2005. Specificity of antibodies: unexpected cross reactivity of antibodies directed against the EAAT3 (EAAC) glutamate transporter. Neuroscience. 136:649-660.
23. Holmseth S, Dehnes Y, Huang YH, Follin-Arbelet VV, Grutle NJ, Mylonakou MN, Plachez C, Zhou Y, Furness DN, Bergles DE, et al. 2012a. The density of EAAC1 (EAAT3) glutamate transporters expressed by neurons in the mammalian CNS. J Neurosci. 32:6000-6013.
24. Holmseth S, Lehre KP, Danbolt NC. 2006. Specificity controls for immunocytochemistry. Anat Embryol (Berl). 211:257-266.
25. Holmseth S, Scott HA, Real K, Lehre KP, Leergaard TB, Bjaalie JG, Danbolt NC. 2009. The concentrations and distributions of three C-terminal variants of the GLT1 (EAAT2; slc1a2) glutamate transporter protein in rat brain tissue suggest differential regulation. Neuroscience. 162:1055-1071.
26. Holmseth S, Zhou Y, Follin-Arbelet V, Lehre K, Bergles D, Danbolt N. 2012b. Specificity controls for immunocytochemistry: the antigen pre-adsorption test can lead to inaccurate assessment of antibody specificity. J Histochem Cytochem. 60:174-187.
27. Jiang J, Amara SG. 2011. New views of glutamate transporter structure and function: advances and challenges. Neuropharmacology. 60:172-181.
28. Kanai Y, Hediger MA. 1992. Primary structure and functional characterization of a high-affinity glutamate transporter. Nature. 360:467-471.
29. Lehre KP, Levy LM, Ottersen OP, Storm-Mathisen J, Danbolt NC. 1995. Differential expression of two glial glutamate transporters in the rat brain: quantitative and immunocytochemical observations. J Neurosci. 15:1835-1853.
30. Leinenweber A, Machtens J-P, Begemann B, Fahlke C. 2011. Regulation of glial glutamate transporters by C-terminal domains. J Biol Chem. 286:1927-1937.
31. Levy LM, Lehre KP, Rolstad B, Danbolt NC. 1993. A monoclonal antibody raised against an [Na+-K+] coupled L-glutamate transporter purified from rat brain confirms glial cell localization. FEBS Lett. 317:79-84.
32. Lorincz A, Nusser Z. 2008. Specificity of immunoreactions: the importance of testing specificity in each method. J Neurosci. 28:9083-9086.
33. Mathern GW, Mendoza D, Lozada A, Pretorius JK, Dehnes Y, Danbolt NC, Nelson N, Leite JP, Chimelli L. 1999. Hippocampal GABA and glutamate transporter immunoreactivity in patients with temporal lobe epilepsy. Neurology. 52:453-472.
34. Matute C, Melone M, Vallejo-Illarramendi A, Conti F. 2005. Increased expression of the astrocytic glutamate transporter GLT-1 in the prefrontal cortex of schizophrenics. Glia. 49:451-455.
35. Melone M, Bellesi M, Conti F. 2009. Synaptic localization of GLT-1a in the rat somatic sensory cortex. Glia. 57:108-117.
36. Melone M, Bellesi M, Ducati A, Iacoangeli M, Conti F. 2011. Cellular and synaptic localization of EAAT2a in human cerebral cortex. Front Neuroanat. 4:151.
37. Melone M, Vitellaro-Zuccarello L, Vallejo-Illarramendi A, Pérez-Samartin A, Matute C, Cozzi A, Pellegrini-Giampietro DE, Rothstein JD, Conti F. 2001. The expression of glutamate transporter GLT-1 in the rat cerebral cortex is down-regulated by the antipsychotic drug clozapine. Mol Psychiatry. 6:380-386.
38. Milton ID, Banner SJ, Ince PG, Piggott NH, Fray AE, Thatcher N, Horne CH, Shaw PJ. 1997. Expression of the glial glutamate transporter EAAT2 in the human CNS: an immunohistochemical study. Brain Res Mol Brain Res. 52:17-31.
39. Münch C, Zhu B-G, Leven A, Stamm S, Einkorn H, Schwalenstocker B, Ludolph AC, Riepe MW, Meyer T. 2003. Differential regulation of 5' splice variants of the glutamate transporter EAAT2 in an in vivo model of chemical hypoxia induced by 3-nitropropionic acid. J Neurosci Res. 71:819-825.
40. Oberheim NA, Takano T, Han X, He W, Lin JH, Wang F, Xu Q, Wyatt JD, Pilcher W, Ojemann JG, et al. 2009. Uniquely hominid features of adult human astrocytes. J Neurosci. 29:3276-3287.
41. Pines G, Danbolt NC, Bjørås M, Zhang Y, Bendahan A, Eide L, Koepsell H, Storm-Mathisen J, Seeberg E, Kanner BI. 1992. Cloning and expression of a rat brain L-glutamate transporter. Nature. 360:464-467.
42. Proper EA, Hoogland G, Kappen SM, Jansen GH, Rensen MG, Schrama LH, van Veelen CW, van Rijen PC, van Nieuwenhuizen O, Gispen WH, de Graan PN. 2002. Distribution of glutamate transporters in the hippocampus of patients with pharmaco-resistant temporal lobe epilepsy. Brain. 125:32-43.
43. Rauen T, Wiessner M, Sullivan R, Lee A, Pow DV. 2004. A new GLT1 splice variant: cloning and immunolocalization of GLT1c in the mammalian retina and brain. Neurochem Int. 45:1095-1106.
44. Reichenbach A, Derouiche A, Kirchhoff F. 2010. Morphology and dynamics of perisynaptic glia. Brain Res Rev. 63:11-25.
45. Schmitt A, Asan E, Puschel B, Kugler P. 1997. Cellular and regional distribution of the glutamate transporter GLAST in the CNS of rats: nonradioactive in situ hybridization and comparative immunocytochemistry. J Neurosci. 17:1-10.
46. Schwarcz R. 1981. Effects of tissue storage and freezing on brain glutamate uptake. Life Sci. 28:1147-1154.
47. Scott HA, Gebhardt FM, Mitrovic AD, Vandenberg RJ, Dodd PR. 2011. Glutamate transporter variants reduce glutamate uptake in Alzheimer's disease. Neurobiol Aging. 32:553. e1-553. e11.
48. Storck T, Schulte S, Hofmann K, Stoffel W. 1992. Structure, expression, and functional analysis of a Na+-dependent glutamate/aspartate transporter from rat brain. Proc Natl Acad Sci U S A. 89:10955-10959.
49. Susarla BT, Robinson MB. 2008. Internalization and degradation of the glutamate transporter GLT-1 in response to phorbol ester. Neurochem Int. 52:709-722.
50. Tanaka K. 1993. Expression cloning of a rat glutamate transporter. Neurosci Res. 16:149-153.
51. Tanaka K, Watase K, Manabe T, Yamada K, Watanabe M, Takahashi K, Iwama H, Nishikawa T, Ichihara N, Hori S, et al. 1997. Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science. 276:1699-1702.
52. Tessler S, Danbolt NC, Faull RLM, Storm-Mathisen J, Emson PC. 1999. Expression of the glutamate transporters in human temporal lobe epilepsy. Neuroscience. 88:1083-1091.
53. Ullensvang K, Lehre KP, Storm-Mathisen J, Danbolt NC. 1997. Differential developmental expression of the two rat brain glutamate transporter proteins GLAST and GLT. Eur J Neurosci. 9:1646-1655.
54. Utsunomiya-Tate N, Endou H, Kanai Y. 1997. Tissue specific variants of glutamate transporter GLT-1. FEBS Lett. 416:312-316.
55. Watase K, Hashimoto K, Kano M, Yamada K, Watanabe M, Inoue Y, Okuyama S, Sakagawa T, Ogawa S, Kawashima N, et al. 1998. Motor discoordination and increased susceptibility to cerebellar injury in GLAST mutant mice. Eur J Neurosci. 10:976-988.
56. Williams SM, Sullivan RK, Scott HL, Finkelstein DI, Colditz PB, Lingwood BE, Dodd PR, Pow DV. 2005. Glial glutamate transporter expression patterns in brains from multiple mammalian species. Glia. 49:520-541.
57. Wilson JM, Khabazian I, Pow DV, Craig UK, Shaw CA. 2003. Decrease in glial glutamate transporter variants and excitatory amino acid receptor down-regulation in a murine model of ALS-PDC. Neuromolecular Med. 3:105-117.
58. Woltjer RL, Duerson K, Fullmer JM, Mookherjee P, Ryan AM, Montine TJ, Kaye JA, Quinn JF, Silbert L, Erten-Lyons D, et al. 2010. Aberrant detergent-insoluble excitatory amino acid transporter 2 accumulates in Alzheimer disease. J Neuropathol Exp Neurol. 69:667-676.
59. Zhou Y, Holmseth S, Hua R, Lehre AC, Olofsson AM, Poblete-Naredo I, Kempson SA, Danbolt NC. 2012. The betaine-GABA transporter (BGT1, slc6a12) is predominantly expressed in the liver and at lower levels in the kidneys and at the brain surface. Am J Physiol Renal Physiol. 302:F316-F328.